Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response

• Published in: Neuron (Cambridge, Mass.) Vol. 97; no. 4; pp. 953 - 966.e8
• Main Authors: Russo, Abigail A., Bittner, Sean R., Perkins, Sean M., Seely, Jeffrey S., London, Brian M., Lara, Antonio H., Miri, Andrew, Marshall, Najja J., Kohn, Adam, Jessell, Thomas M., Abbott, Laurence F., Cunningham, John P., Churchland, Mark M.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 21-02-2018; Elsevier Limited
• Subjects: Activity patterns; Animals; Cortex (motor); Interneurons; Kinematics; Macaca mulatta; Male; Mice; Models, Neurological; Motor Activity; motor control; motor cortex; Motor Cortex - physiology; Motor neurons; Motor Neurons - physiology; Motor task performance; movement generation; Muscle function; Muscle, Skeletal - physiology; neural dynamics; neural network; Neural networks; Neural Pathways - physiology; Neurons; pattern generation; Population; rhythmic movement; United States > US; rhythmic movement; motor cortex; movement generation; neural dynamics; pattern generation; motor control; neural network
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2018.01.004

Primate motor cortex projects to spinal interneurons and motoneurons, suggesting that motor cortex activity may be dominated by muscle-like commands. Observations during reaching lend support to this view, but evidence remains ambiguous and much debated. To provide a different perspective, we employed a novel behavioral paradigm that facilitates comparison between time-evolving neural and muscle activity. We found that single motor cortex neurons displayed many muscle-like properties, but the structure of population activity was not muscle-like. Unlike muscle activity, neural activity was structured to avoid “tangling”: moments where similar activity patterns led to dissimilar future patterns. Avoidance of tangling was present across tasks and species. Network models revealed a potential reason for this consistent feature: low tangling confers noise robustness. Finally, we were able to predict motor cortex activity from muscle activity by leveraging the hypothesis that muscle-like commands are embedded in additional structure that yields low tangling.
•Motor cortex displays a signature of a smooth dynamical system: low tangling•Low tangling explains the previously puzzling dominant signals in motor cortex•Low tangling confers noise robustness and predicts population activity patterns•Motor cortex embeds output commands in structure that reduces tangling
Using a novel extended movement task, Russo et al. show that neural activity in motor cortex is dominated by non-muscle-like signals. A computational approach reveals that these dominant features are expected and can be predicted given the constraint that neural activity produces muscle commands while obeying a smooth flow-field.